A comparative study of ribosomal proteins: linkage between amino acid distribution and ribosomal assembly.

BACKGROUND: Assembly of the ribosome from its protein and RNA constituents must occur quickly and efficiently in order to synthesize the proteins necessary for all cellular activity. Since the early 1960's, certain characteristics of possible assembly pathways have been elucidated, yet the mechanisms that govern the precise recognition events remain unclear.We utilize a comparative analysis to investigate the amino acid composition of ribosomal proteins (r-proteins) with respect to their role in the assembly process. We compared small subunit (30S) r-protein sequences to those of other housekeeping proteins from 560 bacterial species and searched for correlations between r-protein amino acid content and factors such as assembly binding order, environmental growth temperature, protein size, and contact with ribosomal RNA (rRNA) in the 30S complex. RESULTS: We find r-proteins have a significantly high percent of positive residues, which are highly represented at rRNA contact sites. An inverse correlation between the percent of positive residues and r-protein size was identified and is mainly due to the content of Lysine residues, rather than Arginine. Nearly all r-proteins carry a net positive charge, but no statistical correlation between the net charge and the binding order was detected. Thermophilic (high-temperature) r-proteins contain increased Arginine, Isoleucine, and Tyrosine, and decreased Serine and Threonine compared to mesophilic (lower-temperature), reflecting a known distinction between thermophiles and mesophiles, possibly to account for protein thermostability. However, this difference in amino acid content does not extend to rRNA contact sites, as the proportions of thermophilic and mesophilic contact residues are not significantly different. CONCLUSIONS: Given the significantly higher level of positively charged residues in r-proteins and at contact sites, we conclude that ribosome assembly relies heavily on an electrostatic component of interaction. However, the binding order of r-proteins in assembly does not appear to depend on these electrostatics interactions. Additionally, because thermophiles and mesophiles exhibit significantly different amino acid compositions in their sequences but not in the identities of contact sites, we conclude that this electrostatic component of interaction is insensitive to temperature and is not the determining factor differentiating the temperature sensitivity of ribosome assembly.

Population structure, demographic history, and evolutionary patterns of a green-fruited tomato, Solanum peruvianum (Solanaceae), revealed by spatial genetics analyses.

PREMISE OF THE STUDY: Wild relatives of crop species have long been viewed as an important genetic resource for crop improvement, but basic information about the population biology of these species is often lacking. This study investigated the population structure, demographic history, and evolutionary patterns of a green-fruited relative of the cultivated tomato, Solanum peruvianum. METHODS: We investigated spatial genetics of S. peruvianum and screened for loci potentially under natural selection by integrating amplified fragment length polymorphism (AFLP) genotypes, phenotypic data, geography, and geographic information system (GIS)-derived climate data of 19 natural populations. KEY RESULTS: Solanum peruvianum had a moderate degree of population differentiation, likely reflecting partial geographic isolation between species. Populations had a distribution pattern consistent with north-to-south "stepping-stone" dispersal with significant isolation by distance (IBD), similar to other tomato species. Several AFLP loci showed evidence of selection and associated with climate variables. However, phenotypic traits generally did not correlate with climate variables. CONCLUSIONS: Geographic features of the coastal Andes is likely an important factor that determines the migration pattern and population structure of S. peruvianum, but climatic factors do not appear to be critical for its phenotypic evolution, perhaps due to a high degree of phenotypic plasticity. Spatial genetics of wild relatives of crop species is a powerful approach to understand their evolutionary patterns and to accelerate the discovery of their potential for crop improvements.

Spatial genetics of wild tomato species reveals roles of the Andean geography on demographic history.

PREMISE OF THE STUDY: Understanding the demographic history of natural populations in relation to the geographic features in their habitats is an important step toward deciphering the mechanisms of evolutionary processes in nature. This study investigates how the complex geographic and ecological features of the Andes play a role in demographic history, species divergence, dispersal patterns, and hybridization in wild tomato species. METHODS: We investigated spatial genetics of two closely related wild tomato species, Solanum lycopersicum and S. pimpinellifolium, by integrating amplified fragment length polymorphism (AFLP) marker data and geographic information system (GIS)-derived geographic and climatic data. KEY RESULTS: The two species represent genetically distinct lineages largely separated by the Andes, but hybridize extensively in central to northern Ecuador, likely mediated by the transitional climatic conditions between those of the two species. Solanum lycospericum has likely experienced a severe population bottleneck during the colonization of the eastern Andes followed by a rapid population expansion. CONCLUSIONS: The study demonstrates that the evolutionary patterns of the two wild tomatoes, including demographic history, dispersal patterns, interspecific divergence, and hybridization, are intimately related to the complex geographic and ecological features of the Andes. Integrating genetic data across the genome and GIS-derived environmental data can provide insights into the patterns of complex evolutionary processes in nature.

Hybrid incompatibility "snowballs" between Solanum species.

Among the reproductive barriers that can isolate species, hybrid sterility is frequently due to dysfunctional interactions between loci that accumulate between differentiating lineages. Theory describing the evolution of these incompatibilities has generated the prediction, still empirically untested, that loci underlying hybrid incompatibility should accumulate faster than linearly with time--the "snowball effect." We evaluated the accumulation of quantitative trait loci (QTL) between species in the plant group Solanum and found evidence for a faster-than-linear accumulation of hybrid seed sterility QTL, thus empirically evaluating and confirming this theoretical prediction. In comparison, loci underlying traits unrelated to hybrid sterility show no evidence for an accelerating rate of accumulation between species.

Ecological and geographic modes of species divergence in wild tomatoes.

Understanding the role of geography and ecology in species divergence is central to the study of evolutionary diversification. We used climatic, geographic, and biological data from nine wild Andean tomato species to describe each species' ecological niche and to evaluate the likely ecological and geographical modes of speciation in this clade. Using data from >1000 wild accessions and publicly available data derived from geographic information systems for various environmental variables, we found most species pairs were significantly differentiated for one or more environmental variables. By comparing species' predicted niches generated by species distribution modeling (SDM), we found significant niche differentiation among three of four sister-species pairs, suggesting ecological divergence is consistently associated with recent divergence. In comparison, based on age-range correlation (ARC) analysis, there was no evidence for a predominant geographical (allopatric vs. sympatric) context for speciation in this group. Overall, our results suggest an important role for environmentally mediated differentiation, rather than simply geographical isolation, in species divergence.

Complex epistasis for Dobzhansky-Muller hybrid incompatibility in solanum.

We examined the prevalence of interactions between pairs of short chromosomal regions from one species (Solanum habrochaites) co-introgressed into a heterospecific genetic background (Solanum lycopersicum). Of 105 double introgression line (DIL) families generated from a complete diallele combination of 15 chromosomal segments, 39 ( approximately 38%) showed evidence for complex epistasis in the form of genotypic and/or allelic marker transmission distortion in DIL F(2) populations.

Investigating species boundaries in the Giliopsis group of Ipomopsis (Polemoniaceae): Strong discordance among molecular and morphological markers.

As a first step in elucidating mechanisms of speciation in the Giliopsis group of Ipomopsis (Polemoniaceae), we examined patterns of morphological and genetic differentiation and crossability. This group comprises three species that diverged very recently: two perennials, I. guttata and I. tenuifolia, and one annual, I. effusa. Analysis of phenotypic variation established that the three species are distinct for floral characters, and this differentiation is maintained in a locality containing both perennial species. Next, we assessed the genealogical relationships with AFLPs. All sampled individuals of I. effusa clustered together, a result in accord with its genetic isolation. The perennials, which retain interfertility, were not resolved as sister taxa. Rather, individuals sampled from the single I. guttata population that is sympatric with I. tenuifolia were genetically more similar to I. tenuifolia samples than they were to conspecifics. This pattern may be due to substantial introgression of I. tenuifolia genomic regions that do not contribute to floral phenotype in I. guttata. Our result adds to mounting evidence that plant species, as defined by morphological characters, are often not genomically cohesive. Taken together, our data warrant caution in delimiting species with genetic markers alone, and, importantly, suggest that selection on species-diagnostic morphological characters can be sufficiently strong to counteract extensive gene flow.

Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses.

The genetic basis of hybrid sterility can provide insight into the genetic and evolutionary origins of species barriers. We examine the genetics of hybrid incompatibility between two diploid plant species in the plant clade Solanum sect. Lycopersicon. Using a set of near-isogenic lines (NILs) representing the wild species Solanum pennellii (formerly Lycopersicon pennellii) in the genetic background of the cultivated tomato S. lycopersicum (formerly L. esculentum), we found that hybrid pollen and seed infertility are each based on a modest number of loci, male (pollen) and other (seed) incompatibility factors are roughly comparable in number, and seed-infertility QTL act additively or recessively. These findings are remarkably consistent with our previous analysis in a different species pair, S. lycopersicum x S. habrochaites. Data from both studies contrast strongly with data from Drosophila. Finally, QTL for pollen and seed sterility from the two Solanum studies were chromosomally colocalized, indicating a shared evolutionary history for these QTL, a nonrandom genomic distribution of loci causing sterility, and/or a proclivity of certain genes to be involved in hybrid sterility. We show that comparative mapping data can delimit the probable timing of evolution of detected QTL and discern which sterility loci likely evolved earliest among species.

Environmental factors predict adaptive phenotypic differentiation within and between two wild Andean tomatoes.

Environmental variation is widely viewed as a major force driving morphological change and speciation. Although many environmental attributes are potentially critical for adaptive responses within and between species, the individual and relative importance of these diverse attributes remain poorly understood. Here we combine a geographical information systems (GIS)-based analysis of environmental variation with a multipopulation analysis of phenotypic, physiological, and genetic variation, to generate and test hypotheses of environmental factors likely driving adaptive divergence within and between two wild Andean plant species. First, we document large environmental differences between population locations of the two species, and among regions within species. Second, we show evidence for inter- and intraspecific differences in genetically based phenotypic and physiological variation. Third, combining these data, we report evidence for trait-environment associations both among populations within species, and between species, that are strongly indicative of recent and rapid adaptive responses. Finally, we show that these trait-environment associations cannot be simply explained by genetic relatedness within species, reinforcing our inference that local, regional, and species-wide environmental conditions are responsible for phenotypic and physiological diversification. The strongest trait-environment associations involve temperature and precipitation gradients, suggesting these climatic factors are predominant drivers of adaptive diversification in these species.

A genomewide study of reproductive barriers between allopatric populations of a homosporous fern, Ceratopteris richardii.

Biological factors involved in reproductive barriers between two divergent races of Ceratopteris richardii were investigated. We used a combination of spore germination rates, QTL analysis of spore germination rates, and transmission ratio distortion (TRD) of 729 RFLPs, AFLPs, and isozyme markers distributed across the genome on the basis of hybrid populations of 488 doubled haploid lines (DHLs) and 168 F(2)'s. Substantial reproductive barriers were found between the parental races, predominantly in the form of spore inviability (23.7% F(1) spore viability). Intrinsic genetic factors such as Bateson-Dobzhansky-Muller (BDM) incompatibilities involving both nuclear-nuclear and nuclear-cytoplasmic factors and chromosomal rearrangements appear to contribute to intrinsic postzygotic isolation. The genomewide distribution patterns of TRD loci support the hypothesis that reproductive barriers are a byproduct of divergence in allopatry and that the strong reproductive barriers are attributable to a small number of genetic elements scattered throughout the genome.

Genetic map-based analysis of genome structure in the homosporous fern Ceratopteris richardii.

Homosporous ferns have extremely high chromosome numbers relative to flowering plants, but the species with the lowest chromosome numbers show gene expression patterns typical of diploid organisms, suggesting that they may be diploidized ancient polyploids. To investigate the role of polyploidy in fern genome evolution, and to provide permanent genetic resources for this neglected group, we constructed a high-resolution genetic linkage map of the homosporous fern model species, Ceratopteris richardii (n = 39). Linkage map construction employed 488 doubled haploid lines (DHLs) that were genotyped for 368 RFLP, 358 AFLP, and 3 isozyme markers. Forty-one linkage groups were recovered, with average spacing between markers of 3.18 cM. Most loci (approximately 76%) are duplicated and most duplicates occur on different linkage groups, indicating that as in other eukaryotic genomes, gene duplication plays a prominent role in shaping the architecture of fern genomes. Although past polyploidization is a potential mechanism for the observed abundance of gene duplicates, a wide range in the number of gene duplicates as well as the absence of large syntenic regions consisting of duplicated gene copies implies that small-scale duplications may be the primary mode of gene duplication in C. richardii. Alternatively, evidence of past polyploidization(s) may be masked by extensive chromosomal rearrangements as well as smaller-scale duplications and deletions following polyploidization(s).

Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species.

New species may arise via hybridization and without a change in ploidy. This process, termed homoploid hybrid speciation, is theoretically difficult because it requires the development of reproductive barriers in sympatry or parapatry. Theory suggests that isolation may arise through rapid karyotypic evolution and/or ecological divergence of hybrid neospecies. Here, we investigate the role of karyotypic change in homoploid hybrid speciation by generating detailed genetic linkage maps for three hybrid sunflower species, Helianthus anomalus, H. deserticola, and H. paradoxus, and comparing these maps to those previously generated for the parental species, H. annuus and H. petiolaris. We also conduct a quantitative trait locus (QTL) analysis of pollen fertility in a BC2 population between the parental species and assess levels of pollen and seed fertility in all cross-combinations of the hybrid and parental species. The three hybrid species are massively divergent from their parental species in karyotype; gene order differences were observed for between 9 and 11 linkage groups (of 17 total), depending on the comparison. About one-third of the karyoypic differences arose through the sorting of chromosomal rearrangements that differentiate the parental species, but the remainder appear to have arisen de novo (six breakages/six fusions in H. anomalus, four breakages/three fusions in H. deserticola, and five breakages/five fusions in H. paradoxus). QTL analyses indicate that the karyotypic differences contribute to reproductive isolation. Nine of 11 pollen viability QTL occur on rearranged chromosomes and all but one map close to a rearrangement breakpoint. Finally, pollen and seed fertility estimates for F1's between the hybrid and parental species fall below 11%, which is sufficient for evolutionary independence of the hybrid neospecies.

Comparative mapping and rapid karyotypic evolution in the genus helianthus.

Comparative genetic linkage maps provide a powerful tool for the study of karyotypic evolution. We constructed a joint SSR/RAPD genetic linkage map of the Helianthus petiolaris genome and used it, along with an integrated SSR genetic linkage map derived from four independent H. annuus mapping populations, to examine the evolution of genome structure between these two annual sunflower species. The results of this work indicate the presence of 27 colinear segments resulting from a minimum of eight translocations and three inversions. These 11 rearrangements are more than previously suspected on the basis of either cytological or genetic map-based analyses. Taken together, these rearrangements required a minimum of 20 chromosomal breakages/fusions. On the basis of estimates of the time since divergence of these two species (750,000-1,000,000 years), this translates into an estimated rate of 5.5-7.3 chromosomal rearrangements per million years of evolution, the highest rate reported for any taxonomic group to date.

Major ecological transitions in wild sunflowers facilitated by hybridization.

Hybridization is frequent in many organismal groups, but its role in adaptation is poorly understood. In sunflowers, species found in the most extreme habitats are ancient hybrids, and new gene combinations generated by hybridization are speculated to have contributed to ecological divergence. This possibility was tested through phenotypic and genomic comparisons of ancient and synthetic hybrids. Most trait differences in ancient hybrids could be recreated by complementary gene action in synthetic hybrids and were favored by selection. The same combinations of parental chromosomal segments required to generate extreme phenotypes in synthetic hybrids also occurred in ancient hybrids. Thus, hybridization facilitated ecological divergence in sunflowers.